Transmission Dynamics of Borrelia turicatae from the Arthropod Vector

Abstract

BackgroundWith the global distribution, morbidity, and mortality associated with tick and louse-borne relapsing fever spirochetes, it is important to understand the dynamics of vector colonization by the bacteria and transmission to the host. Tick-borne relapsing fever spirochetes are blood-borne pathogens transmitted through the saliva of soft ticks, yet little is known about the transmission capability of these pathogens during the relatively short bloodmeal. This study was therefore initiated to understand the transmission dynamics of the relapsing fever spirochete Borrelia turicatae from the vector Ornithodoros turicata, and the subsequent dissemination of the bacteria upon entry into murine blood.Methodology/Principal FindingsTo determine the minimum number of ticks required to transmit spirochetes, one to three infected O. turicata were allowed to feed to repletion on individual mice. Murine infection and dissemination of the spirochetes was evaluated by dark field microscopy of blood, quantitative PCR, and immunoblotting against B. turicatae protein lysates and a recombinant antigen, the Borrelia immunogenic protein A. Transmission frequencies were also determined by interrupting the bloodmeal 15 seconds after tick attachment. Scanning electron microscopy (SEM) was performed on infected salivary glands to detect spirochetes within acini lumen and excretory ducts. Furthermore, spirochete colonization and dissemination from the bite site was investigated by feeding infected O. turicata on the ears of mice, removing the attachment site after engorment, and evaluating murine infection.Conclusion/SignificanceOur findings demonstrated that three ticks provided a sufficient infectious dose to infect nearly all animals, and B. turicatae was transmitted within seconds of tick attachment. Spirochetes were also detected in acini lumen of salivary glands by SEM. Upon host entry, B. turicatae did not require colonization of the bite site to establish murine infection. These results suggest that once B. turicatae colonizes the salivary glands the spirochetes are preadapted for rapid entry into the mammal.

Imaging of Borrelia turicatae Producing the Green Fluorescent Protein Reveals Persistent Colonization of the Ornithodoros turicata Midgut and Salivary Glands from Nymphal Acquisition through Transmission

“…Depending on the life stage, Ornithodoros species complete the blood meal within five to 60 min (9), and a full blood meal is not required for RF spirochete transmission (4). Transmission kinetics indicate that there is insufficient time for the midgut population to migrate to the salivary glands and enter the vertebrate host.…”

“…Two current systems used to study the tick-mammal transmission cycle of RF spirochetes include the Borrelia hermsii-Ornithodoros hermsi and Borrelia turicataeOrnithodoros turicata models (4)(5)(6). These models demonstrated initial midgut colonization following an infectious blood meal, and in the following weeks, spirochetes migrated to colonize the salivary glands (6,7).…”

“…These models demonstrated initial midgut colonization following an infectious blood meal, and in the following weeks, spirochetes migrated to colonize the salivary glands (6,7). Given the tick's short blood meal duration, the salivary gland population is important to continue the pathogen's life cycle in the mammal (4,8). Moreover, after tick feeding and through the molt, RF spirochetes are maintained transstadially (8,9).…”

Do Tick Attachment Times Vary between Different Tick-Pathogen Systems?

“…Based on documented differences in engorgement periods, pathogen transmission by soft ticks may occur more rapidly than via hard ticks. Others have shown a dose-dependent relationship for successful pathogen transmission demonstrated by simultaneous blood feeding by multiple soft ticks (e.g., three Ornithodoros turicata Duges start transmitting Borrelia turicatae to mice within 15-40 s (tick-borne relapsing fever)) [31].…”

Correction: Vol. 16, No. 1

“…There is overlap of bacterial, viral, and parasitic pathogens in location and nonspecific symptom presentations. The O. turicata tick bite is rarely noticed or reported because the vectors are rapid nocturnal feeders, attachment is painless, and often no lesions or ticks are discovered (10). This case report with successful isolation and genetic characterization of B. turicatae from the soldier (3) confirms that this spirochete species is a zoonotic pathogen.…”